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Phenotypic differences in reversible attachment behavior reveal distinct P. aeruginosa surface colonization strategies

View ORCID ProfileCalvin K. Lee, Jérémy Vachier, Jaime de Anda, Kun Zhao, Amy E. Baker, Rachel R. Bennett, Catherine R. Armbruster, Kimberley A. Lewis, Rebecca L. Tarnopol, Charles J. Lomba, Deborah A. Hogan, Matthew R. Parsek, George A. O’Toole, Ramin Golestanian, Gerard C. L. Wong
doi: https://doi.org/10.1101/798843
Calvin K. Lee
1Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA 90095-1600, USA
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  • ORCID record for Calvin K. Lee
Jérémy Vachier
2Max Planck Institute for Dynamics and Self-Organization (MPIDS), Am Fassberg 17, D-37077 Göttingen, Germany
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Jaime de Anda
1Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA 90095-1600, USA
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Kun Zhao
3Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Collaborative Innovation Center of Chemical Science and Engineering, Tianjin University, Tianjin 300072, People’s Republic of China
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Amy E. Baker
4Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH 03755, USA
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Rachel R. Bennett
5School of Mathematics, University of Bristol, Bristol BS8 1TW, UK
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Catherine R. Armbruster
6Department of Microbiology, University of Washington, Seattle, Washington 98195, USA
9Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15219
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Kimberley A. Lewis
4Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH 03755, USA
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Rebecca L. Tarnopol
7Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720-3102, USA
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Charles J. Lomba
1Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA 90095-1600, USA
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Deborah A. Hogan
4Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH 03755, USA
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Matthew R. Parsek
6Department of Microbiology, University of Washington, Seattle, Washington 98195, USA
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George A. O’Toole
4Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH 03755, USA
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Ramin Golestanian
2Max Planck Institute for Dynamics and Self-Organization (MPIDS), Am Fassberg 17, D-37077 Göttingen, Germany
8Rudolf Peierls Centre for Theoretical Physics, University of Oxford, Oxford OX1 3PU, United Kingdom
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  • For correspondence: gclwong@seas.ucla.edu ramin.golestanian@ds.mpg.de
Gerard C. L. Wong
1Department of Bioengineering, Department of Chemistry and Biochemistry, and California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA 90095-1600, USA
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  • For correspondence: gclwong@seas.ucla.edu ramin.golestanian@ds.mpg.de
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Abstract

Despite possessing the machinery to sense, adhere to, and proliferate on surfaces, it is commonly observed that bacteria initially have a difficult time attaching to a surface. Before forming a bacterial biofilm, planktonic bacteria exhibit a random period of transient surface attachment known as “reversible attachment” which is poorly understood. Using community tracking methods at single-cell resolution, we examine how reversible attachment progresses during initial stages of surface sensing. Pseudomonas aeruginosa strains PAO1 and PA14, which exhibit similar exponential trends of surface cell population increase, show unanticipated differences when the behavior of each cell was considered at the full lineage level and interpreted using the unifying quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two complementary surface colonization strategies, which are roughly analogous to “immediate-” vs “deferred-gratification” in a prototypical cognitive-affective processing system. PAO1 lineages commit relatively quickly to a surface compared to PA14 lineages. PA14 lineages allow detaching cells to retain memory of the surface so that they are primed for improved subsequent surface attachment. In fact, it is possible to identify motility suppression events in PA14 lineages in the process of surface commitment. We hypothesize that these contrasting strategies are rooted in downstream differences between Wsp-based and Pil-Chp-based surface sensing systems.

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Posted October 10, 2019.
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Phenotypic differences in reversible attachment behavior reveal distinct P. aeruginosa surface colonization strategies
Calvin K. Lee, Jérémy Vachier, Jaime de Anda, Kun Zhao, Amy E. Baker, Rachel R. Bennett, Catherine R. Armbruster, Kimberley A. Lewis, Rebecca L. Tarnopol, Charles J. Lomba, Deborah A. Hogan, Matthew R. Parsek, George A. O’Toole, Ramin Golestanian, Gerard C. L. Wong
bioRxiv 798843; doi: https://doi.org/10.1101/798843
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Phenotypic differences in reversible attachment behavior reveal distinct P. aeruginosa surface colonization strategies
Calvin K. Lee, Jérémy Vachier, Jaime de Anda, Kun Zhao, Amy E. Baker, Rachel R. Bennett, Catherine R. Armbruster, Kimberley A. Lewis, Rebecca L. Tarnopol, Charles J. Lomba, Deborah A. Hogan, Matthew R. Parsek, George A. O’Toole, Ramin Golestanian, Gerard C. L. Wong
bioRxiv 798843; doi: https://doi.org/10.1101/798843

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